Title: Induced spermiation of<i>Pimelodus britskii</i>(Teleostei: Pimelodidae) during the reproductive period
Abstract: Aquaculture ResearchVolume 48, Issue 3 p. 862-874 Original Article Induced spermiation of Pimelodus britskii (Teleostei: Pimelodidae) during the reproductive period Danielle Zanerato Damasceno, Corresponding Author Danielle Zanerato Damasceno [email protected] Centro de Aquicultura da Universidade Estadual Paulista "Júlio de Mesquita Filho", Jaboticabal, SP, BrazilCorrespondence: D Z Damasceno, Rua da Faculdade, 645, La Salle, Toledo, Paraná, CEP, Brazil. E-mail: [email protected]Search for more papers by this authorRicardo Andrei Krause, Ricardo Andrei Krause Universidade Estadual do Oeste do Paraná, Toledo, PR, BrazilSearch for more papers by this authorMaurício Spagnolo Adames, Maurício Spagnolo Adames Universidade Estadual do Oeste do Paraná, Toledo, PR, BrazilSearch for more papers by this authorGiovano Neumann, Giovano Neumann Universidade Estadual do Oeste do Paraná, Toledo, PR, BrazilSearch for more papers by this authorAnderson Gibathe, Anderson Gibathe TRACTEBEL Energia, UHE Salto Santiago, Saudade do Iguaçu, PR, BrazilSearch for more papers by this authorRobie Allan Bombardelli, Robie Allan Bombardelli Universidade Estadual do Oeste do Paraná, Toledo, PR, BrazilSearch for more papers by this authorElizabeth Romagosa, Elizabeth Romagosa Instituto de Pesca-APTA, SAA, SP, BrazilSearch for more papers by this author Danielle Zanerato Damasceno, Corresponding Author Danielle Zanerato Damasceno [email protected] Centro de Aquicultura da Universidade Estadual Paulista "Júlio de Mesquita Filho", Jaboticabal, SP, BrazilCorrespondence: D Z Damasceno, Rua da Faculdade, 645, La Salle, Toledo, Paraná, CEP, Brazil. E-mail: [email protected]Search for more papers by this authorRicardo Andrei Krause, Ricardo Andrei Krause Universidade Estadual do Oeste do Paraná, Toledo, PR, BrazilSearch for more papers by this authorMaurício Spagnolo Adames, Maurício Spagnolo Adames Universidade Estadual do Oeste do Paraná, Toledo, PR, BrazilSearch for more papers by this authorGiovano Neumann, Giovano Neumann Universidade Estadual do Oeste do Paraná, Toledo, PR, BrazilSearch for more papers by this authorAnderson Gibathe, Anderson Gibathe TRACTEBEL Energia, UHE Salto Santiago, Saudade do Iguaçu, PR, BrazilSearch for more papers by this authorRobie Allan Bombardelli, Robie Allan Bombardelli Universidade Estadual do Oeste do Paraná, Toledo, PR, BrazilSearch for more papers by this authorElizabeth Romagosa, Elizabeth Romagosa Instituto de Pesca-APTA, SAA, SP, BrazilSearch for more papers by this author First published: 14 December 2015 https://doi.org/10.1111/are.12930Citations: 4Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract For the first time was characterized the semen of Pimelodus britskii, hormonally induced and non-induced induced, during the reproductive period. The experiment 1 was conducted with 12 fish per month, divided into: (i) induced with Carp Pituitary Extract (CPE), and (ii) without hormonal induction (testes macerated). The experiment 2 was conducted, with 30 fish, divided into groups for comparison of different doses of CPE and human Chorionic Gonadotrophin (hCG; T1: control; T2: 3.0 mg kg−1 CPE; T3: 0.5 mg kg + 3.0 mg kg−1 CPE; T4: 0.5 mg kg−1 + 7.0 mg kg−1 CPE; T5: 200 UI kg−1 hCG), the same fish were used every month, and the semen was collected by abdominal massage. In both, experiments were assessed the sperm motility and velocity by means of the CASA software. In experiment 1, the concentration of spermatozoids was significantly increase by application of CPE compared untreated males. The volume and motility decreased gradually until the end of the experiment, the highest values were recorded for treatment induced (0.49 ± 0.25 mL and 62.18, respectively). The same occurred to Gonadosomatic Index, showing the smallest value at the end of the reproductive period. The fish from experiment 2 released reduced volume of watery semen (0.1 mL). The values of sperm concentration, motility velocity decreased gradually throughout the months. For P. britskii, the reproductive period influenced the production and sperm quality. Despite small seminal volume released the dose of 7.5 mg kg−1 of CPE proved effective. References Alavi S.M.H. & Cosson J.J. (2005) Sperm motility in fishes. I. Effects of temperatureand pH: a review. Cell Biology International 29, 101–110. 10.1016/j.cellbi.2004.11.021 PubMedWeb of Science®Google Scholar Alavi S.M.H., Psenicka M., Rodina M., Policar T. & Linhart O. (2008) Changes of sperm morphology, volume, density and motility and seminal plasma composition in Barbus barbus (Teleostei: Cyprinidae) during the reproductive season. Aquatic Living Resour 21, 75–80. 10.1051/alr:2008011 Web of Science®Google Scholar Arantes F.P., Borçato F.L., Sato Y., Rizzo E. & Bazzoli N. (2013) Reproduction and embryogenesis of the mandi-amarelo catfish (Pisces, Pimelodidae), in captivity. Anatomia Histologia Embryologia 42, 30–39. 10.1111/j.1439-0264.2012.01160.x CASPubMedWeb of Science®Google Scholar Asturiano J.F., Sorbera L.A., Carrilo M., Zanuy S., Ramos J., Navarro J.C. & Bromage N. (2001) Reproductive performance in male European sea bass (Dicentrarchus labrax, L.) fed two PUFA—enriched experimental diets: a comparison with males fed a wet diet. Aquaculture 194, 173–190. 10.1016/S0044-8486(00)00515-9 CASWeb of Science®Google Scholar Asturiano F., Marco-Jiménez F., Peréz L., Balasch S., Garzón D.L., Peñaranda D.S., Vicente J.S., Viudes-de-Castro M.P. & Jover M. (2006) Effects of hCG as spermiation inducer on European eel semen quality. Theriogenology 66, 1012–1102. 10.1016/j.theriogenology.2006.02.041 CASPubMedWeb of Science®Google Scholar Batlouni S.R., Carreño F.R., Romagosa E. & Borella M.I. (2005) Cell junctions in the germinal epithelium may play an important role in spermatogenesis of the catfish Pseudoplatystoma fasciatum (Pisces, Siluriformes). Journal of Molecular Hystology 36, 97–110. 10.1007/s10735-004-4115-0 CASPubMedWeb of Science®Google Scholar Batlouni S.R., Romagosa E. & Borella M.I. (2006) The reproductive cycle of male catfish Pseudoplatystoma fasciatum (Teleostei, Pimelodidae) revealed by changes of the germinal epithelium an approach addressed to aquaculture. Animal Reproduction Science 96, 116–132. 10.1016/j.anireprosci.2005.11.012 CASPubMedWeb of Science®Google Scholar Baumgartner G., Pavanelli C.S., Baumgartner D., Bifi A.G., Debona T. & Frana V.A. (2012) Peixes do Baixo Rio Iguaçu. Eduem, Maringá, Brazil. 10.7476/9788576285861 Google Scholar Bombardelli R.A., Mörschbächer E.F., Campagnolo R., Sanches E.A. & Syperreck M.A. (2006) Dose inseminante para fertilização artificial de ovócitos de jundiá Rhamdia quelen (Quoy & Gaimardm, 1824). Revista Brasileira de Zootecnia 35, 1251–1257. 10.1590/S1516-35982006000500001 Web of Science®Google Scholar Cabrita E., Robles V. & Harráez P. (2008) Sperm quality assessment. In: Methods in Reproductive Aquaculture: Marine and Freshwater Species (ed. by E. Cabrita, V. Robles & P. Herráez), pp. 93–147. Taylor & Francis Groups, New York, USA. 10.1201/9780849380549 Google Scholar Cacot P., Eeckhoutte P., Muon D.T., Trieu N.V., Legendre M., Mariojouls C. & Lazard J. (2003) Induced spermiation and milt management in Pangasius bocourti (Sauvage, 1880). Aquaculture 215, 67–77. 10.1016/S0044-8486(02)00032-7 Web of Science®Google Scholar Caneppele D. (2011) Steindachneridion parahybae (Steindachner, 1876) (Siluriformes: Pimelodidae): produção espermática ao longo de um ciclo reprodutivo. Dissertação apresentada ao Programa de Pós-graduação em Aquicultura e Pesca do Instituto de Pesca, APTA - SAA, como parte dos requisitos para obtenção do titulo de Mestre em Aquicultura e Pesca. 70p. Google Scholar CBRA (Colégio Brasileiro De Reprodução Animal) (1998) Manual para exame andrológico e avaliação de sêmen animal ( 2nd edn). CBRA, Belo Horizonte, Minas Gerais, Brazil. Google Scholar Cejko B.I., Kowalski R.K., Zarski D., Dryl K., Targonska K., Chwaluczyk R., Kucharczyk D. & Glogowski J. (2012) The influence of the length of time after hormonal treatment with [(D-Ala6, Pro9NEt)-mGnRH metoclopramide] i.e. Ovopel on barbel Barbus barbus (L.) milt quality and quantity indicators. Journal Applied of Ichthyology 28, 249–253. 10.1111/j.1439-0426.2011.01923.x Web of Science®Google Scholar Cejko B.I., Zarski D., Judycka S., Kucharczyk D., Sarosiek B. & Kowalski R.K. (2013) Effect of two commercial preparations containing different GnRH analogues with dopamine antagonists on barbel Barbus barbus (L.) sperm quantity and quality. Aquaculture International 22, 97–109. 10.1007/s10499-013-9657-2 CASWeb of Science®Google Scholar Cejko B.I., Krejszeff S., Judycka S., Sarosiek B., Dietrich M., Kucharczyk D. & Kowalski R.K. (2014) Sperm quality and selected biochemical markers of seminal plasma at the beginning of the reproductive period of common carp, Cyprinus carpio L. Aquaculture International 22, 111–122. 10.1007/s10499-013-9672-3 CASWeb of Science®Google Scholar CFMV (Conselho Federal de Medicina Veterinária) (2008) Resolução n° 876, de 15-02-2008, publicada no DOU de 25-02-2008. Seção 1, p. 100. Google Scholar Cosson J. (2010) Frenetic activation of fish spermatozoa flagella entails short-term motility, portending their precocious decadence. Journal of Fish Biology 76, 240–279. 10.1111/j.1095-8649.2009.02504.x CASPubMedWeb of Science®Google Scholar Diemer O., Bittencourt F., Barcellos L.G., Boscolo W.R., Feidin A. & Romagosa E. (2014) Lysine in the diet of Rhamdia voulezi male broodstocks confined in net cages. Aquaculture 434, 93–99. 10.1016/j.aquaculture.2014.07.029 CASWeb of Science®Google Scholar Ferreira A.A., Nuñer A.P.O., Luz R.K., Tataje D.A.R., Esquivel J.R. & Restrepo J.B. (2001) Avaliação qualitativa e quantitativa do sêmen do jundiá, Rhamdia quelen. Boletim do Instituto de Pesca 27, 57–60. Google Scholar Garavello J.C. & Shibatta O.A. (2007) A new species of the genus Pimelodus (LA CÉPÈDE, 1803) from do rio Iguaçu basin and a reappraisal of (Pimelodus ortmani) (Haseman, 1911) from de rio Paraná system, Brazil (Ostariophysi: Siluriformes: Pimelodidae). Neotropical Ichthyology 5, 282–292. 10.1590/S1679-62252007000300008 Web of Science®Google Scholar Gima M.E., Gima A., Hutson A., Chaimongkol A., Beam R., Perera D.A. & Dunham R.A. (2013) Realized heritability and response to selection for fecundity, hatching rate and fry/Kg for channel catfish females (Ictalurus punctatus) induced to ovulate and fertilized with blue catfish (Ictalurus furcatus) males for the production of hybrid catfish embryos. Aquaculture 420–421 (Suppl. 1), s36–s41. Google Scholar Guerrero H.Y., Cardillo E., Poleo G. & Marcano D. (2009) Reproductive biology of freshwater fishes from the Venezuelan floodplains. Fish Physiology Biochemical 35, 189–196. 10.1007/s10695-008-9249-7 CASPubMedWeb of Science®Google Scholar Legendre M., Linhart O. & Billard R. (1996) Spawning and management of gametes, fertilized eggs and embryos in Siluroidei. Aquatic Living Research 9, 59–80. 10.1051/alr:1996042 Web of Science®Google Scholar Leonardo A.F.G., Romagosa E., Borella M.I. & Batlouni S.R. (2004) Induced spawning of hatchery-raised Brazilian catfish, cachara Pseudoplatystoma fasciatum (Linnaeus, 1766). Aquaculture 240, 451–461. 10.1016/j.aquaculture.2003.11.030 Web of Science®Google Scholar Loir M., Cauty C., Planquette P. & Le Bail P.Y. (1989) Comparative study of the male reproductive tract in seven families of South-American catfishes. Aquatic Living Resource 2, 45–56. 10.1051/alr:1989005 Google Scholar Luz R.K., Ferreira A.A., Reynalte D.A.T. & Zaniboni-Filho E. (2001) Avaliação qualitativa e quantitativa do sêmen de suruvi, Steindachneridion scripta (Pimelodidae). Boletim do Instituto de Pesca 27, 39–42. Google Scholar Mañanos E., Duncan N. & Mylonas C.C. (2008) Reproduction and control of ovulation, spermiation and spawning in cultured fish. In: Methods in Reproductive Aquaculture: Marine and Freshwater Species (ed. by E. Cabrita, V. Robles & M.P. Herráez), pp. 3–80. CRC Press, Taylor and Francis Group, Boca Raton, FL, USA. Google Scholar Mansour N., Ramoun A. & Lahnsteiner F. (2005) Quality of testicular semen of the African catfish Clarias gariepinus (Burchell, 1822) and its relationship with fertilization and hatching success. Aquaculture Research 36, 1422–1428. 10.1111/j.1365-2109.2005.01363.x Web of Science®Google Scholar Maria A.N., Azevedo H.C., Santos J.P. & Carneiro P.C.F. (2011) Hormonal induction and semen characteristics of tambaqui Colossoma macropomum. Zygote 20, 39–43. 10.1017/S0967199410000559 CASPubMedWeb of Science®Google Scholar Melo R.M.C., Arantes F.P., Sato Y., Santos J.E., dos Rizzo E. & Bazzoli N. (2011) Comparative morphology of the gonadal structure related to reproductive strategies in six species of neotropical catfishes (Teleostei: Siluriformes). Journal of Morphology 272, 525–535. 10.1002/jmor.10931 PubMedWeb of Science®Google Scholar Miranda L.A., Cassará M.C. & Somoza G.M. (2005) Increase in milt production by hormonal treatment in the pejerrey fish Odontesthes bonariensis (Valenciennes 1835). Aquaculture Research 36, 1473–1479. 10.1111/j.1365-2109.2005.01357.x CASWeb of Science®Google Scholar Mylonas C.C., Fostier A. & Zanuy S. (2010) Broodstock management and hormonal manipulations of fish reproduction. General and Comparative Endocrinology 165, 516–534. 10.1016/j.ygcen.2009.03.007 CASPubMedWeb of Science®Google Scholar Nogueira L.B., Azevedo P.G., Canelhas M.R., Bedore A.G., Lopes J.M. & Godinho H.P. (2012) Induced spawning and early ontogeny in hatchery-reared catfish Zungaro jahu (Siluriformes: Pimelodidae). Neotropical Ichthyology 10, 89–98. 10.1590/S1679-62252012000100009 Web of Science®Google Scholar Ohta H. & Tanaka H. (1997) Relationship between serum levels of human chorionic gonadotropin (hCG) and 11-ketotestosterone after a single injection of hCG and induced maturity in the male Japanes eel, Anguilla japonica. Aquaculture 153, 123–134. 10.1016/S0044-8486(97)00020-3 CASWeb of Science®Google Scholar Pan J., Ding S., Ge J., Yan W., Hao C., Chen J. & Huang Y. (2008) Development of cryopreservation for maintaining yellow catfish Pelteobagrus fulvidraco sperm. Aquaculture 279, 173–176. 10.1016/j.aquaculture.2008.03.037 CASWeb of Science®Google Scholar Perchec G., Jeulin C., Cosson J., André F. & Billard F. (1995) Relationship between sperm ATP content and motility of carp spermatozoa. Journal of Cell Science 108, 747–753. 10.1242/jcs.108.2.747 CASPubMedWeb of Science®Google Scholar Perchec G., Cosson M.P., Cosson J., Jeulin C. & Billard R. (1996) Morphological and kinetic sperm changes of carp (Cyprinus carpio) spermatozoa after initiation of motility in distilled water. Cell Motility and the Cytoskeleton 35, 113–120. 10.1002/(SICI)1097-0169(1996)35:2<113::AID-CM4>3.0.CO;2-B CASPubMedWeb of Science®Google Scholar Poupard G.P., Paxion C. & Cosson J. (1998) Initiation of carp spermatozoa motility and early ATP reduction after milt contamination by urine. Aquaculture 160, 317–328. 10.1016/S0044-8486(97)00301-3 CASWeb of Science®Google Scholar Romagosa E. (2006) Biologia reprodutiva e fisiologia de peixes em confinamento: o cachara, Pseudoplatystoma fasciatum como modelo. In: Tópicos Especiais em Biologia Aquática e Aquicultura (ed. by J.E.P. Cyrino & E.C. Urbinati), pp. 107–116. Sociedade Brasileira de Aquicultura e Biologia Aquática, Jaboticabal, São Paulo, Brazil. Google Scholar Romagosa E. (2008) Avanços na reprodução de peixes migradores. In: Tópicos Especiais em Biologia Aquática e Aqüicultura (ed. by J.E.P. Cyrino & E.C. Urbinati), pp. 1–16. Sociedade Brasileira de Aquicultura e Biologia Aquática, Jaboticabal, São Paulo, Brasil. Google Scholar Romagosa E. (2010) Reproductive status in females of the Brazilian catfish, Pseudoplatystoma fasciatum reared in cages. Journal Applied Ichthyology 26, 806–811. 10.1111/j.1439-0426.2010.01532.x Web of Science®Google Scholar Rurangwa E., Volckaert F.A.M., Huyskens G., Kime D.E. & Ollevier F. (2000) Quality control of refrigerated and cryopreserved semen using Computer-Assisted Sperm Analysis (CASA), viable staining and standardized fertilization in African catfish (Clarias gariepinus). Theriogenology 55, 751–769. 10.1016/S0093-691X(01)00441-1 Web of Science®Google Scholar Sanches E.A., Bombardelli R.A., Marcos R.M., Neumann G., Toledo C.P.R. & Romagosa E. (2010) Sperm motility of Rhamdia quelen studied using computer-assisted analysis by open-source software. Aquaculture Research 42, 153–156. 10.1111/j.1365-2109.2010.02598.x Web of Science®Google Scholar Sanches E.A., Bombardelli R.A., Baggio D.M., Sykora R.M. & Xavier A.M.M. (2011) Características seminais do cascudo-preto (Rhinelepis aspera). Revista Brasileira de Reprodução Animal 35, 357–362. Google Scholar Sanches E.A., Neumann G., Toledo C.P.R., Bombardelli R.A., Piana P.A. & Romagosa E. (2013) Temperature and storage period over spermatic parameters of jundia′, Rhamdia quelen (Quoy & Gaimard, 1824). Aquaculture Research 44, 534–541. 10.1111/j.1365-2109.2011.03056.x Web of Science®Google Scholar Sanches E.A., Marcos R.M., Okawara R.Y., Caneppele D., Bombardelli R.A. & Romagosa E. (2013) Sperm motility parameters for Steindachneridion parahybae based on open-source software. Journal Applied of Ichthyology 29, 1114–1122. 10.1111/jai.12165 Web of Science®Google Scholar Santos J.E., Bazzoli N., Rizzo E. & Santos G.B. (2001) Morphofunctional organization of the male reproductive system of the catfish Iheringichthys labrosus (Lu Ètken, 1874) (Siluriformes:Pimelodidae). Tissue and Cell 33, 533–540. 10.1054/tice.2001.0207 CASPubMedWeb of Science®Google Scholar Sato Y., Fenerich-Verani N., Verani J.R., Godinho H.P. & Sampaio E.V. (1999) Reproductive traits of the yellow-mandi catfish Pimelodus maculatus Lacepede (Osteichthyes, Siluriformes) in captive breeding. Revista Brasileira de Zoologia 16, 981–986. 10.1590/S0101-81751999000400006 Google Scholar Sato Y., Fenerich-Verani N. & Godinho H.P. (2003) Reprodução induzida de peixes da bacia do São Francisco. In: Água, peixes e pescadores do São Francisco das Minas Gerais (ed. by H.P. Godinho & A.L. Godinho), pp. 275–289. Editora PUCMinas, Belo Horizonte, Brasil. Google Scholar Scorvo Filho J.D. (2008) Piscicultura em tanques-rede uma alternativa para grandes e pequenos corpos d'água. In: AveSui América Latina, Avesui, Florianópolis, Brasil. Google Scholar Shibatta O.A., Novelli J.L., Dias J.H.P., Britto S.G.C. & Filho M.C. (2011) Reprodução em cativeiro do jurupecê Sorubim lima (Siluriformes, Pimelodidae) por meio de indução hormonal. Semina: Ciências Agrárias 32, 363–372. 10.5433/1679-0359.2011v32n1p363 Web of Science®Google Scholar Targońska K. & Kucharczyk D. (2011) The application of hCG, CPH and ovopel in successful artificial reproduction of goldfish (Carassius auratus auratus) under controlled conditions. Reproduction Domestic Animals 46, 651–655. 10.1111/j.1439-0531.2010.01723.x CASPubMedWeb of Science®Google Scholar Tessaro L., Toledo C.P.R., Neumann G., Krause R.A., Meurer F., Natali M.R.M. & Bombardelli R.A. (2012) Growth and reproductive characteristics of Rhamdia quelen males fed on different digestible energy levels in the reproductive phase. Aquaculture 326–329, 74–80. 10.1016/j.aquaculture.2011.11.012 Web of Science®Google Scholar Viveiros A.T.M. & Godinho H.P. (2009) Sperm quality and cryopreservation of Brazilian freshwater fish species: a review. Fish Physiology and Biochemistry 35, 137–150. 10.1007/s10695-008-9240-3 CASPubMedWeb of Science®Google Scholar Viveiros A.T.M., Fessehaye Y., ter Veld M., Schulz R.W. & Komen J. (2002) Hand-stripping of semen and semen quality after maturational hormone treatments, in African catfish Clarias gariepinus. Aquaculture 213, 373–386. 10.1016/S0044-8486(02)00036-4 CASWeb of Science®Google Scholar Viveiros A.T.M., Jatzkowski A. & Komen J. (2003) Effect of oxytocin on semen release response in African catfish (Clarias gariepinus). Theriogenology 59, 1905–1917. 10.1016/S0093-691X(02)01290-6 CASPubMedWeb of Science®Google Scholar Viveiros A.T.M., Gonçalves A.C.S., Di Chiacchio I.M., Nascimento A.F., Romagosa E. & Leal M.C. (2013) Gamete quality of streaked prochilod Prochilodus lineatus (Characiformes) after GnRHa and dopamine antagonista treatment. Zygote 23, 1–10. PubMedWeb of Science®Google Scholar Wilson-Leedy J.G. & Ingermann R.L. (2007) Development of a novel CASA system based on open source software for characterization of zebrafish sperm motility parameters. Theriogenology 67, 661–672. 10.1016/j.theriogenology.2006.10.003 PubMedWeb of Science®Google Scholar Zaniboni-Filho E. & Nuñer A.P.O. (2004) Fisiologia da reprodução e propagação artificial dos peixes. In: Tópicos Especiais em Piscicultura de Água Doce Tropical Intensiva (ed. by J.E.P. Cyrino, E.C. Urbinati, D.M. Fracalossi & N. Castagnolli). TecArt, São Paulo, Brazil. Google Scholar Zohar Y. & Mylonas C.C. (2001) Endocrine manipulations of spawning in cultured fish: from hormones to genes. Aquaculture 197, 99–136. 10.1016/S0044-8486(01)00584-1 CASWeb of Science®Google Scholar Citing Literature Volume48, Issue3March 2017Pages 862-874 ReferencesRelatedInformation